Abstract
Digenean trematode distributions, compatibility profiles with their snail hosts, and complete life cycles remain mysteries in many parts of the world. Surveys of digenean biology and ecology provide further insight and perspective into just how incredibly diverse and important helminth parasites are in shaping local ecosystems. Past surveys have provided substantial characterizations of adult digeneans within their definitive hosts, and many now have contributed toward furthering our understanding of larval digeneans within their intermediate host communities. However, much information about the diversity of digeneans and their relationships with their snail intermediate hosts are lacking in many locations across the globe. This is certainly true in Canada, where few records related to digenean-snail relationships exist. Currently, there is a need for more information about the presence and distribution of digeneans across Canada, and how this compares to other parts of North America and beyond. To address this diversity gap in Western Canada, six lakes within central Alberta were surveyed for the presence of snails and larval digenean species and their associations. This investigation into the diversity of digeneans utilized a combined approach of morphological and molecular tools to identify 39 digenean species among five snail host species, from biweekly collections, taken over the course of 2 years (2013–2014). Here, digenean-snail combinations, presence, and distribution across sampling sites and lakes are reported. Overall, this survey contributes new information toward digenean-snail compatibility, life cycles, and distribution in Northern lake ecosystems within North America.
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References
Baldwin RE, Goater CP (2003) Circulation of parasites among fishes from lakes in the Caribou Mountains, Alberta, Canada. J Parasitol 89:215–25. doi:10.1645/0022-3395(2003)089[0215:COPAFF]2.0.CO;2
Bayne CJ, Hahn UK, Bender RC (2001) Mechanisms of molluscan host resistance and of parasite strategies for survival. Parasitology 123(Suppl):S159–67. doi:10.1017/S0031182001008137
Besansky NJ, Severson DW, Ferdig MT (2003) DNA barcoding of parasites and invertebrate disease vectors: what you don’t know can hurt you. Trends Parasitol 19:545–6
Blankespoor HD (1974) Host-induced variation in Plagiorchis noblei Park, 1936 (Plagiorchiidae: Trematoda). Am Midl Nat 92:415. doi:10.2307/2424306
Brant SV, Loker ES (2009) Molecular systematics of the avian schistosome genus Trichobilharzia (Trematoda: Schistosomatidae) in North America. J Parasitol 95:941–63. doi:10.1645/GE-1870.1
Bursey CR, Goldberg SR (1998) Helminths of the Canadian toad, Bufo hemiophrys (Amphibia: Anura), from Alberta, Canada. J Parasitol 84:617–8
Bush AO, Holmes JC (1986) Intestinal helminths of lesser scaup ducks: an interactive community. Can J Zool 64:142–52
Clifford HF (1991) Aquatic Invertebrates of Alberta: An Illustrated Guide. University of Alberta
R Core Team (2015) R: A Language and Environment for Statistical Computing.
Cribb T (1997) Guide to the parasites of fishes of Canada. Part IV. Trematoda. Int J Parasitol 27:1115
Detwiler JT, Bos DH, Minchella DJ (2010) Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Mol Phylogenet Evol 55:611–20. doi:10.1016/j.ympev.2010.01.004
Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Colloquium paper: homage to Linnaeus: how many parasites? How many hosts? Proc Natl Acad Sci U S A 105:11482–9. doi:10.1073/pnas.0803232105
Donald K, Kennedy M, Poulin R, Spencer HG (2004) Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). Int J Parasitol 34:557–68
Faltýnková A, Nasincová V, Kablásková L (2008) Larval trematodes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in Central Europe: a survey of species and key to their identification. Syst Parasitol 69:155–78. doi:10.1007/s11230-007-9127-1
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–9. doi:10.1371/journal.pone.0013102
Georgieva S, Selbach C, Faltýnková A, Soldanova M, Sures B, Skirnisson K, Kostadinova A (2013) New cryptic species of the “revolutum” group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasit Vectors 6:64
Georgieva S, Faltýnková A, Brown R, Blasco-Costa I, Soldánová M, Sitko J, Scholz T, Kostadinova A (2014) Echinostoma ʻrevolutumʼ (Digenea: Echinostomatidae) species complex revisited: species delimitation based on novel molecular and morphological data. Parasit Vectors 7:520
Gibson DI (1987) Questions in digenean systematics and evolution. Parasitology 95:429–60
Gibson DI, Bray RA (1994) The evolutionary expansion and host-parasite relationships of the Digenea. Int J Parasitol 24:1213–26
Giebelhaus IT, Kennedy MJ, Moraiko DT (1998) First report of Fasciola hepatica in cattle in Alberta. Can Vet J 39:433
Goldberg SR, Bursey CR, Wong C (2002) Helminths of the western chorus frog from eastern Alberta, Canada. Northwest Sci 76:77–9
Gustafson KD, Kensinger BJ, Bolek MG, Luttbeg B (2014) Distinct snail (Physa) morphotypes from different habitats converge in shell shape and size under common garden conditions. Evol Ecol Res 16:77–89
Hair JD, Holmes JC (1970) Helminths of Bonaparte’s gulls, Larus philadelphia, from Cooking Lake, Alberta. Can J Zool 48:1129–31
Hanington PC, Forys MA, Loker ES (2012) A Somatically Diversified Defense Factor, FREP3, Is a Determinant of Snail Resistance to Schistosome Infection. PLoS Negl Trop Dis. doi: ARTN e1591DOI 10.1371/journal.pntd.0001591
Hechinger RF, Lafferty KD (2005) Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. Proc Biol Sci 272:1059–66. doi:10.1098/rspb.2005.3070
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical J 50:346–63
Hudson PJ, Dobson AP, Lafferty KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol 21:381–5. doi:10.1016/j.tree.2006.04.007
Johnson PTJ, Preston DL, Hoverman JT, LaFonte BE (2013) Host and parasite diversity jointly control disease risk in complex communities. Proc Natl Acad Sci U S A 110:16916–21. doi:10.1073/pnas.1310557110
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–9. doi:10.1093/bioinformatics/bts199
Králová-Hromadová I, Bazsalovicsová E, Štefka J, Špakulová M, Vávrová S, Szemes T, Tkach VV, Trudgett A, Pybus M (2011) Multiple origins of European populations of the giant liver fluke Fascioloides magna (Trematoda: Fasciolidae), a liver parasite of ruminants. Int J Parasitol 41:373–83. doi:10.1016/j.ijpara.2010.10.010
Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J, Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R, Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–46. doi:10.1111/j.1461-0248.2008.01174.x
Lawton SP, Lim RM, Dukes JP, Kett SM, Cook RT, Walker AJ, Kirk RS (2015) Unravelling the riddle of Radix: DNA barcoding for species identification of freshwater snail intermediate hosts of zoonotic digeneans and estimating their inter-population evolutionary relationships. Infect Genet Evol 35:63–74. doi:10.1016/j.meegid.2015.07.021
Leong TS, Holmes JC (1981) Communities of metazoan parasites in open water fishes of Cold Lake, Alberta. J Fish Biol 18:693–713. doi:10.1111/j.1095-8649.1981.tb03811.x
Littlewood DTJ, Bray RA (2001) Interrelationships of the Platyhelminthes. In: Littlewood DTJ, Bray RA (eds). Taylor & Francis
Locke SA, McLaughlin JD, Marcogliese DJ (2010) DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater. Mol Ecol 19:2813–27
Locke SA, McLaughlin JD, Lapierre AR, Johnson PTJ, Marcogliese DJ (2011) Linking larvae and adults of Apharyngostrigea cornu, Hysteromorpha triloba, and Alaria mustelae (Diplostomoidea: Digenea) using molecular data. J Parasitol 97:846–51. doi:10.1645/GE-2775.1
Lowenberger C, Rau M (1994) Plagiorchis elegans: emergence, longevity and infectivity of cercariae, and host behavioural modifications during cercarial emergence. Parasitology 109:65–72
Loy C, Haas W (2001) Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitol Res 87:878–82
Morningstar CR, Inoue K, Sei M, Lang BK, Berg DJ (2014) Quantifying morphological and genetic variation of sympatric populations to guide conservation of endangered, micro-endemic springsnails. Aquat Conserv Mar Freshw Ecosyst 24:536–45. doi:10.1002/aqc.2422
Morris JR, Boag DA (1982) On the dispersion, population structure, and life history of a basommatophoran snail, Helisoma trivolvis, in central Alberta. Can J Zool 60:2931–40
Moszczynska A, Locke SA, McLaughlin JD, Marcogliese DJ, Crease TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Mol Ecol Resour 9(Suppl s1):75–82. doi:10.1111/j.1755-0998.2009.02634.x
Nadler S, DE León G (2011) Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138:1688–709
Palmieri JR (1973) New definitive and intermediate hosts and host localities for Apatemon gracilis (Rud, 1819) Szidat, 1928. J Parasitol 59:1063
Ramalingam S, Samuel WM (1978) Helminths in the great horned owl, Bubo virginianus, and snowy owl, Nyctea scandiaca, of Alberta. Can J Zool 56:2454–6. doi:10.1139/z78-331
Rubinoff D, Cameron S, Will K (2006) A genomic perspective on the shortcomings of mitochondrial DNA for “barcoding” identification. J Hered 97:581–94. doi:10.1093/jhered/esl036
Samuel WM, Barrett MW, Lynch GM (1976) Helminths in moose of Alberta. Can J Zool 54:307–12. doi:10.1139/z76-034
Sankurathri CS, Holmes JC (1976) Effects of thermal effluents on parasites and commensals of Physa gyrina Say (Mollusca: Gastropoda) and their interactions at Lake Wabamun, Alberta. Can J Zool 54:1742–53. doi:10.1139/z76-202
Sapp KK, Loker ES (2000a) A comparative study of mechanisms underlying digenean-snail specificity: In vitro interactions between hemocytes and digenean larvae. J Parasitol 86:1020–9. doi:10.1645/0022-3395(2000)086[1020:Acsomu]2.0.Co;2
Sapp KK, Loker ES (2000b) Mechanisms underlying digenean-snail specificity: role of miracidial attachment and host plasma factors. J Parasitol 86:1012–9. doi:10.1645/0022-3395(2000)086[1012:Mudssr]2.0.Co;2
Schell SC (1985) Handbook of the trematodes of North America north of Mexico. University Press Idaho, Moscow (Idaho)
Schleppe JL, Goater CP (2004) Comparative life histories of two diplostomid trematodes, Ornithodiplostomum ptychocheilus and Posthodiplostomum minimum. J Parasitol 90:1387–90. doi:10.1645/GE-274R
Selbach C, Solda M, Georgieva S, Kostadinova M, Kalbe M, Sures B (2014) Morphological and molecular data for larval stages of four species of Petasiger Dietz, 1909 (Digenea : Echinostomatidae) with an updated key to the known cercariae from the Palaearctic. Syst Parasitol 89:153–66. doi:10.1007/s11230-014-9513-4
Shostak AW (1993) Survival of Petasiger nitidus (Digenea: Echinostomatidae) cercariae in relation to temperature, pH, and salinity. Can J Zool 71:431–4
Shostak AW, Dharampaul S, Belosevic M (1993) Effects of source of metacercariae on experimental infection of Zygocotyle lunata (Digenea: Paramphistomidae) in CD-1 mice. J Parasitol 79:922–9
Stock TM, Holmes JC (1988) Functional relationships and microhabitat distributions of enteric helminths of grebes (Podicipedidae): the evidence for interactive communities. J Parasitol 74:214–27
Tkach VV (2008) Family Plagiorchiidae Lühe, 1901. In: Bray R, Gison D, Jones A (eds) Keys to the Trematoda, vol 3, CAB International. Cambridge, UK, pp 295–325
Tkach VV, Pawlowski J, Sharpilo V (2000) Molecular and morphological differentiation between species of the Plagiorchis vespertilionis group (Digenea, Plagiorchiidae) occurring in European bats, with a re- description of P. vespertilionis (Müller, 1780). Syst Parasitol 47:9–22
Ulmer MJ (1970) Notes on rearing of snails in the laboratory. In: Experiments and techniques in paraSsitology. W. H. Freeman and Co. San Francisco, pp 143–144
UNEP (2015) Sourcebook of opportunities for enhancing cooperation among the Biodiversity-related Conventions at national and regional levels. Nairobi, Kenya
Van Steenkiste N, Locke SA, Castelin M, Marcogliese DJ, Abbott CL (2015) New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Mol Ecol Resour 15:945–52. doi:10.1111/1755-0998.12358
Vázquez DP, Poulin R, Krasnov BR, Shenbrot GI (2005) Species abundance and the distribution of specialization in host–parasite interaction networks. J Anim Ecol 74:946–55
Vázquez DP, Melian CJ, Williams NM, Bluthgen N, Krasnov BR, Poulin R (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–7. doi:10.1111/J.2007.0030-1299.15825.X
Vermeer K (1969) Comparison of the helminth fauna of California gulls, Larus californicus, and ring-billed gulls, Larus delawarensis, at Beaverhill and Miquelon Lakes, Alberta. Can J Zool 47:267–70. doi:10.1139/z69-057
Vilas R, Criscione C, Blouin M (2005) A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131:1–8
Webster BL (2009) Isolation and preservation of schistosome eggs and larvae in RNAlater(R) facilitates genetic profiling of individuals. Parasit Vectors 2:50. doi:10.1186/1756-3305-2-50
Whiteman NK, Parker PG (2005) Using parasites to infer host population history: a new rationale for parasite conservation. Anim Conserv 8:175–81. doi:10.1017/S1367943005001915
Wood CL, Johnson PTJ (2015) A world without parasites: exploring the hidden ecology of infection. Front Ecol Environ 13:425–34. doi:10.1890/140368
Zelmer DA, Arai HP (1998) The contributions of host age and size to the aggregated distribution of parasites in yellow perch, Perca flavescens, from Garner Lake, Alberta, Canada. J Parasitol 84:24–8
Acknowledgments
We thank Alethe Kabore, Emmanuel Pila, Walter Gordy, and Sheila Merritt for their assistance in field collections. Special thanks to Zhuoyan Song and Dr. Lien Luong for help with statistical analyses and R programming, and to W. Gordy for help with Python programming to make data analysis more efficient. We thank Dr. Luong and the reviewers for their editorial assistance. This work was funded by Alberta Innovates Energy and Environment Solutions grant 2078 and NSERC 418540 (PCH).
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Supplementary Figure 1
Venn diagrams of unique and shared species. a) Represents the numbers of digenean species unique and shared across lakes, adjusted to only include lakes Wabamun, Isle, Gull, and Buffalo. B) Represents the numbers of unique and shared digenean species across snail species. (GIF 70 kb)
Supplementary Figure 2
Frequency heat-map table of snail and digenean combinations found in central Alberta lakes. Rows describe digenean species and the number found to be infecting each snail species as distinguished by columns. The dotted line separates the samples from which there is sequence information on the top from those in which descriptions are based on morphology alone on the bottom. Column titles: Ht = Helisoma trivolvis, Pa = Planorbula armigera*, Pg = Physella gyrina, Ls = Lymnaea stagnalis, and Se = Stagnicola elodes. (GIF 354 kb)
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Gordy, M.A., Kish, L., Tarrabain, M. et al. A comprehensive survey of larval digenean trematodes and their snail hosts in central Alberta, Canada. Parasitol Res 115, 3867–3880 (2016). https://doi.org/10.1007/s00436-016-5152-9
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DOI: https://doi.org/10.1007/s00436-016-5152-9